Hidden in the sand: Comparative venomics provide insights into the complex venom system of antlions

The antlions are certainly one of the most iconic and peculiar families among the net-winged insects. Hidden in their typical funnel-shaped pitfall traps in the sand, they wait patiently for other arthropods to fall into their trap. Once the unfortunate prey entered the trap, there is usually no escape. The antlion quickly grabs it with its strong pincers and injects potent venom that quickly paralyzes and kills even large, defensive prey. The antlion then drags the prey into the sand and can take the time to pre-digest and suck out the liquefied tissues. Of course, antlions also value cleanliness – after the meal, the carcass is thrown out of the funnel with precision and the antlion is ready for its next victim.

The European antlion Euroleon nostras uses pitfall traps and potent venom to catch prey arthropods. Photo: Benjamin Weiss

The composition and source of the antlions’ venom has been the subject of controversy in the past. While some studies state that they inject gut regurgitant into their prey, others describe the presence of specialized venom glands in the pincers and the head. Moreover, previous studies reported the presence of bacterial gut symbionts that produce the toxins responsible for rapidly paralyzing the antlions’ prey – a rather unusual role of symbionts not described elsewhere in insects. Overall, the existing literature is rather confusing and contradictory. We wanted to clarify this seeming conundrum and finally decipher the venom system of the larvae of the European antlion Euroleon nostras. Where does the venom come from and do antlions really rely on gut symbionts to produce the paralyzing toxins? 
Luckily, as the Department of Insect Symbiosis, we are specialized in finding and localizing all kinds of microbial symbionts in insects. We were of course very excited when we got our hands on the first antlions and were able to start our analyses, but all the more surprised when we discovered that antlions do not harbor any viable bacteria, neither in the gut nor in any other tissues. Instead, we found that all proteins in the antlion’s venom are produced by the insect itself, without the contribution of microbial symbionts. Moreover, antlions turned out to have an impressively complex venom system consisting of three different glands. Our results show that these three glands produce distinct venom mixtures, indicating functional compartmentalization. In insects, the spatial separation of different venoms has so far only been described in true bugs, which use different venoms from different glands for predation and defense, respectively. Although the ecological role of venom compartmentalization in antlions is not clear, the complexity of their venom system is quite remarkable and offers many opportunities for further research.
Antlions live in dry and sandy habitats where they rely on toxic venom to catch also large and defensive prey including ants. In contrast, the larvae of the closely related green lacewing Chrysoperla carnea feed on small, non-defensive prey such as aphids or insect eggs and are likely less dependent on toxic venom. We wondered if the venom composition and activity of these two species reflect their adaptations to different ecological niches and the associated diverging needs. Indeed, we found that the European antlion produces a much more complex and more toxic venom than the green lacewing. Even small amounts of antlion venom reliably induced rapid paralysis and death when injected into insects. This shows that antlions have in fact evolved towards more toxic venom than lacewings to fit their requirements to quickly paralyze and kill large prey – which is crucial to survive in prey-scarce habitats where antlions live.
Our results show that antlions rely on a complex and potent venom mixture to capture prey, but the compounds responsible for the toxic effects are not known. We identified a number of novel proteins in the antlion venom that are not known from other animals, including the closely-related green lacewing. The characterization of these proteins is particularly interesting as they may have toxic functions that the antlion needs to survive in its harsh habitats. Moreover, these compounds may have different targets and modes of action than other insect toxins, and could contribute to the discovery of novel insecticides and be helpful for medical research. We therefore aim to further characterize the venom compounds of the European antlion and are looking forward to the discoveries and surprises that these hidden creatures still have in store.
 

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